Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
ABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investiga...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00091-18 |
| _version_ | 1818742216009449472 |
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| author | Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis |
| author_facet | Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis |
| author_sort | Adrien Vigneron |
| collection | DOAJ |
| description | ABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCE Cold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction. |
| first_indexed | 2024-12-18T02:08:59Z |
| format | Article |
| id | doaj.art-396eebc8155e4e69b48ca07d53fe64f2 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-18T02:08:59Z |
| publishDate | 2019-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-396eebc8155e4e69b48ca07d53fe64f22022-12-21T21:24:31ZengAmerican Society for MicrobiologymSystems2379-50772019-02-014110.1128/mSystems.00091-18Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep SedimentsAdrien Vigneron0Eric B. Alsop1Perrine Cruaud2Gwenaelle Philibert3Benjamin King4Leslie Baksmaty5David Lavallee6Bartholomeus P. Lomans7Emiley Eloe-Fadrosh8Nikos C. Kyrpides9Ian M. Head10Nicolas Tsesmetzis11School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomShell International Exploration and Production Inc., Houston, Texas, USADepartement de Biochimie, de Microbiologie, et de Bio-Informatique, Faculté des Sciences et de Génie, Université Laval, Quebec City, Quebec, CanadaShell International Exploration and Production Inc., Houston, Texas, USAShell International Exploration and Production Inc., Houston, Texas, USAShell International Exploration and Production Inc., Houston, Texas, USAShell International Exploration and Production Inc., Houston, Texas, USAShell Global Solutions International B.V., Rijswijk, NetherlandsDOE Joint Genome Institute, Walnut Creek, California, USADOE Joint Genome Institute, Walnut Creek, California, USASchool of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomSchool of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomABSTRACT Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCE Cold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.https://journals.asm.org/doi/10.1128/mSystems.00091-18AOMmetagenomicmetatranscriptomicmethanepolysulfide |
| spellingShingle | Adrien Vigneron Eric B. Alsop Perrine Cruaud Gwenaelle Philibert Benjamin King Leslie Baksmaty David Lavallee Bartholomeus P. Lomans Emiley Eloe-Fadrosh Nikos C. Kyrpides Ian M. Head Nicolas Tsesmetzis Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments mSystems AOM metagenomic metatranscriptomic methane polysulfide |
| title | Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments |
| title_full | Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments |
| title_fullStr | Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments |
| title_full_unstemmed | Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments |
| title_short | Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments |
| title_sort | contrasting pathways for anaerobic methane oxidation in gulf of mexico cold seep sediments |
| topic | AOM metagenomic metatranscriptomic methane polysulfide |
| url | https://journals.asm.org/doi/10.1128/mSystems.00091-18 |
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